Reproductive competence: a recurrent logic module in eukaryotic development

Abstract

Developmental competence is the ability to differentiate in response to an appropriate stimulus, as first elaborated by Waddington in relation to organs and tissues. Competence thresholds operate at all levels of biological systems from the molecular (e.g. the cell cycle) to the ontological (e.g. metamorphosis and reproduction). Reproductive competence, an organismal process, is well studied in mammals (sexual maturity) and plants (vegetative phase change), though far less than later stages of terminal differentiation. The phenomenon has also been documented in multiple species of multicellular fungi, mostly in early, disparate literature, providing a clear example of physiological differentiation in the absence of morphological change. This review brings together data on reproductive competence in Ascomycete fungi, particularly the model filamentous fungus Aspergillus nidulans, contrasting mechanisms within Unikonts and plants. We posit reproductive competence is an elementary logic module necessary for coordinated development of multicellular organisms or functional units. This includes unitary multicellular life as well as colonial species both unicellular and multicellular (e.g. social insects such as ants). We discuss adaptive hypotheses for developmental and reproductive competence systems and suggest experimental work to address the evolutionary origins, generality and genetic basis of competence in the fungal kingdom.

Keywords: competence; development; fungi; life history; reproduction; vegetative phase change.

Figure 1.

Aspergillus nidulans reproductive cycles and the logic of competence. (a) Depiction of the four reproductive cycles [13]—asexual, sexual, parasexual (producing recombinant haploid nuclei) and hyphal growth (producing clonal nuclei, although replication errors may contribute to heterokaryosis in a mycelium of sufficient size)—all of which may occur simultaneously in a single colony. (b) Developmental timing in A. nidulans for a single, isolated conidium growing at 37°C in the presence of excess, preferred nutrients [12]. (c) Defining competence in A. nidulans [14]. Conidiophores per colony plotted over time since inoculation, in response to variable time of induction (black arrows). Development was induced by exposure of single spore-derived colonies to air and light. Minimum time to conidiation (blue arrow) comprises competence acquisition (grey arrow) and a constant maturation period for conidiophore production (red arrows). Vegetative growth continues indefinitely in the absence of induction and the presence of sufficient nutrients.

Figure 2.

Reproductive competence in Trichoderma and Penicillium species. (a) The relationship between age and conidiation capacity in Trichoderma viride [52]. At left, colonies grown on filter papers were fixed and stained with cotton blue at time of induction by light. At right, duplicate photoinduced colonies after a further 40 h incubation in the dark. A ring of conidia is visible at the colony fringe for colonies of age 20 h or greater. (b) Identification of density dependence for development of Penicillium notatum (chrysogenum) [53]. Inoculum load (conidia per ml of medium) is plotted against sporulation time (induced by addition of calcium) and dry weight at time of sporulation. A minimum of 17.5 h is required under these conditions for sporulation. In other experiments, it was found that 6 h is required for conidiophore production (maturation), regardless of inoculum load. (c) The mevalonate pathway produces key primary and secondary metabolites in diverse species [54]. The diterpenoid competence hormone, conidiogenone, from Penicillium cyclopium is an effector of both competence acquisition and conidiation induction in this species [55].

Figure 3.

Vegetative phase change and transcriptional regulatory networks. Two examples of distinct morphologies associated with vegetative phases in plants. (a) Growth habit and leaf shape in English ivy (Hedera helix) for juvenile (lower) and adult (upper) phases [68]. (b) Melocactus intortus juvenile body (lower) and (upper) the adult apical cephalium [69]. (c) Conserved transcriptional networks controlling phase change in plants [70]. Sugars regulate levels of microRNA miR156, which in turn determines expression of the SPL family of transcription factors required for phase change and flowering.